THE CENTRAL ROLE OFTAXONOMY IN THE STUDY OFNEOTROPICAL BIODIVERSITY1

Laura P. Lagomarsino2* and Laura A. Frost2

ABSTRACT

The Neotropics are the most species-rich area of the planet. Understanding the origin and maintenance of this diversity is animportant goal of ecology and evolutionary biology. Success in this endeavor relies heavily on the past work of taxonomists who havecollected specimens and produced the floras and monographs that constitute the foundation for the study of plant diversity. Toillustrate this, we visualize collecting efforts through time and identify the importance of past taxonomic and collection efforts ingenerating the bulk of specimen data that broad-scale analyses rely on today. To demonstrate the importance of taxonomy for thestudy of Neotropical biodiversity, we showcase selected plant groups in which in-depth taxonomic understanding has facilitatedexciting evolutionary and ecological research and highlight the teams of scientists who have built on the legacy of Alwyn Gentry,one of the most prolific taxonomists of the late 20th century. We also discuss challenges faced by taxonomists, including perceivedsubjectivity, difficulty in measuring impact, and the need to become more interdisciplinary. We end with potential solutions goingforward, including integration of taxonomists in interdisciplinary research, advocacy for continued collection efforts, increasedfunding for alpha taxonomic research that is performed with increasingly replicable methodology, and explicit decolonizationefforts to increase inclusivity and equity in the field of taxonomy. Acknowledging the central role of taxonomy and taxonomists isessential to accurately and completely describe Neotropical biodiversity patterns in an age of unprecedented extinction risk andconservation need.

Key words: Biodiversity, Central America, decolonialization, floristics, herbarium, monography, museum-based research,South America, taxonomic impediment.

For centuries, scientists have tried to understand thedistribution of life on earth and why some geographicregions house much higher species diversity thanothers. The latitudinal species diversity gradient, withspecies richness being highest surrounding the equatorand decreasing toward the poles (Hawkins, 2001), is aclassic area of inquiry. Likewise, the high species rich-ness in the Neotropics compared to other tropical regionsof the globe has inspired innumerable research programs(see Antonelli & Sanmartın, 2011). Understanding theorigin and maintenance of this exceptional biodiversityis a fundamental aim of ecology and evolutionary biologytoday (Antonelli et al., 2017).It is not surprising that these questions have attracted

researchers across subfields, many of which werehighlighted in the 66th Annual Fall Symposium of theMissouri Botanical Garden. Evolutionary studies, includ-ing phylogeographic analyses of widespread taxa that

demonstrate the importance of dispersal barriers instructuring genetic diversity (Dick & Heuertz, 2008;Nazareno et al., 2017) and clade-focused phylogeneticstudies that make a case for both biotic and abioticfactors in driving diversification across the Neotropics(Lagomarsino et al., 2016), shed light on the origin ofthis biodiversity. On more recent time scales, commu-nity ecology provides insights into the coexistence ofspecies in diverse communities (Eck et al., 2019) andthe role of environmental gradients in structuring plantphenotypic diversity (Umaña & Swenson, 2019), both ofwhich are likely tied to plant secondary chemistry(Sedio, 2017) and regional attributes (Ricklefs & He,2016). These studies demonstrate how extant biodi-versity is maintained. Paleobiology further links majorchanges in climate and landscape, such as mountainuplift and changes in drainage systems, to shifts inbiodiversity over deep geological timescales (Claramunt

1 L. P. L. would like to thank Monica Carlsen, Sebastian Tello, and James Miller, the organizers of the 66th Annual FallSymposium of the Missouri Botanical Garden, for their hard work in assembling a diverse lineup of speakers, and for including heramong them. L. P. L.’s time at MO between 2015 and 2017, funded by a National Science Foundation Postdoctoral ResearchFellowship in Biology (grant no. 1523880), shapedmany of the ideas presented here, especially conversations with: TomCroat, RoyGereau, Michael Grayum, Ivan Jimenez, Ron Leisner, Jim Miller, Rosa Ortiz-Gentry, John Pruski, Jim Solomon, Peter Stevens,Charlotte Taylor, Carmen Ulloa-Ulloa, Henk van der Werff, and Jim Zarucchi†. Even while these individuals may have beeninfluential to our thinking, they certainly may not agree with everything we have written. Lucia Lohmann, Doug Daly, Paul Fine,and Sandra Knapp provided invaluable comments that resulted in an appreciably better, more balanced manuscript, and, asalways, conversations and comments from Daniel Santamarıa-Aguilar resulted in further improvements. L. P. L. and L. A. F. arefunded by a grant from the Louisiana Board of Regents Research Competitiveness Subprogram. We dedicate this manuscript to allNeotropical plant taxonomists, past and present, who have devoted their lives to cataloging the most species-rich area of the world,thereby providing the basis for our current understanding about the biodiversity of this incredibly diverse region.

2 Shirley C. Tucker Herbarium, Department of Biological Sciences, Louisiana State University, Baton Rouge, Louisiana, U.S.A.* Author for correspondence: llagomarsino1@lsu.edu

VERSION OF RECORD FIRST PUBLISHED ONLINE ON 30 SEPTEMBER 2020 AHEAD OF FALL 2020 ISSUE.doi: 10.3417/2020601 ANN. MISSOURI BOT. GARD. 105: 405–421.

& Cracraft, 2015), and recent millennia (Pupim et al.,2019; Akesson et al., 2020).The study of Neotropical biodiversity patterns is

becoming increasingly interdisciplinary, merging tech-niques from various subdisciplines (Ribas et al., 2012;Bacon et al., 2015; Salazar et al., 2018; Hoorn et al.,2019). The robust community that studies Neotropicalbiodiversity benefits immensely from the past work oftaxonomists (Mori, 1992). Indeed, these professionalsare often the unsung heroes in broad studies of biodi-versity. The floras and monographs that they authorand the collections they make in the field represent theprimary resources for biodiversity documentation. Like-wise, their hypotheses about species limits are testedexplicitly by molecular systematists and represent thebasic working units used by ecologists. Furthermore,their deep understanding of specific taxa and/or re-gional biodiversity has inspired many studies.Even though taxonomists provide the foundation work

to biodiversity science, their contributions are oftenunder-recognized. For example, even though speciesidentification is crucial to reproducibility (Por, 2007)and determination can be incredibly time-consuming(Mori, 1992), taxonomists’ identifications are rarelyacknowledged in publications. Likewise, the checklists,floras, and monographs that inspire so many ecologicalprojects and from which data are mined for large-scalestudies often go uncited, devaluing the massive amountof labor necessary to compile those lists. Further, thebotanists who collect the bulk of contemporary herbar-ium specimens see no benefit in their profile or reachrelative to those that do not voucher their research.Here, we argue that without foundational knowledge

of alpha taxonomy, the research featured in the 66thsymposium of the Missouri Botanical Garden would nothave been possible. It is thus appropriate that manyspeakers honored Alwyn Gentry’s scientific legacy.Gentry’s hypotheses remain a cornerstone in the studyof Neotropical biodiversity; perhaps less widely known,Gentry was also one of the most prolific taxonomists ofthe late 20th century (Miller et al., 1996).

THE TAXONOMIC IMPEDIMENT AND THE IMPORTANCE OF

EXPERT KNOWLEDGE

One of the most important goals of biology is toproduce a complete inventory of all Earth’s biodiversity,including a list of all of species found on Earth anda comprehensive Tree of Life (Cardoso et al., 2011;Hinchliff et al., 2015). Many exciting developments inthe last half century, including molecular phyloge-netics, phylogenomics, and large-scale natural historycollection digitization efforts, have pushed the bound-aries of systematics in exciting new ways (Sauquet &Graham, 2016). This has resulted in a much more

refined understanding of relationships among organ-isms, facilitating broad comparative analyses that haveshed light on the generalities of the evolutionary process(Hinchliff et al., 2015; Diaz et al., 2019; One ThousandPlant Transcriptomes Initiative, 2019). However, basicmonographic work, the foundation of all biodiversitystudies (Heywood, 2001), has not kept pace, with es-timates suggesting that this branch of study has beeneither in decline or in a period of relative stagnation inrecent decades (Heywood, 2001; Tancoigne & Dubois,2013; Bebber et al., 2014; Miralles et al., 2020). This isdespite the complementary nature of these subdisci-plines of systematics. Indeed, while phylogeneticiststest hypotheses formulated by taxonomists and pub-lished in monographs, taxonomists re-circumscribe taxato reflect the evolutionary relationships published byphylogeneticists.The ability to accurately name species and to de-

scribe new diversity as it is discovered is key to un-derstanding broad biodiversity patterns. However, thesubset of researchers who are trained to do this is small,and is actually shrinking as many experts head intoretirement without guaranteed lines to replace them(Gaston & May 1992; Buyck, 1999). This illustratesthe taxonomic impediment (Cardoso et al., 2017), whichrefers to the disconnect between the diminishing pool ofresearchers who generate floristic inventories and maketaxonomic decisions, and those who use them. Lack ofbasic taxonomic understanding has measurable conse-quences. First, it means that only a small subset of thebiology community has the skills to identify organisms,especially in species-rich tropical regions, and a result-ingly small subset can describe new diversity as it isencountered (Wheeler, 2020). Second, it implies thatchanging taxonomic concepts are curated by a relativelysmall number of employed taxonomists, each with anecessarily narrow realm of specialty, leading to mas-sive numbers of misidentified specimens in herbaria(Goodwin et al., 2015). This is perhaps exacerbated bythe increased reliance on specimens from plot inven-tories for understanding ecology of Neotropical ecosys-tems. While these studies generate important data thatare directly connected to herbarium vouchers, up to50% of these specimens are thought to be erroneouslyidentified (Baker et al., 2017), perhaps in part becausethey rely initially on identifications made by paratax-onomists (Basset et al., 2004).There are crucial consequences of the taxonomic

impediment in the study of global diversity patterns.While macro-ecological and evolutionary studies rely onexhaustive lists of species in different geographic re-gions and biomes, incorrect identifications abound inlarge databases (e.g., iDigBio, GBIF). Misidentificationsin these datasets can lead to significant errors in large-scale studies, including incorrect richness estimates and

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species identity (Cardoso et al., 2017), overestimation ofspecies richness in poorly explored areas (Maldonadoet al., 2015), and inaccurate species distribution models(Oleas et al., 2019). Indeed, Cardoso et al. (2017)documented up to 40% error rate in non-taxonomicallyverified checklists aggregated from publicly availabledatabases. Inaccurate datasets are a clear threat to theaccurate understanding of broad patterns of biodiversity.Even though they entail significant investments of timeand personnel, every attempt to use large databases inbiodiversity studies should involve detailed taxonomicverification and various data-cleaning procedures.

HERBARIA AS A SOURCE OF DIVERSE DATA TYPES TO STUDYTHE PAST, PRESENT, AND FUTURE OF BIODIVERSITY

One of the most exciting changes in the study ofbiodiversity in recent years is a resurgence in the use ofmuseums and specimen-derived data in a broad rangeof biological inquiry. This has been bolstered by speci-fic funding programs by the U.S. National ScienceFoundation (NSF), including the Postdoctoral ResearchFellowships in Biology “Interdisciplinary Research UsingCollections,” “Advancing Digitization of BiodiversityData,” and “Planetary Biodiversity Inventories” pro-grams. Outside of the United States, the digitization ofhistoric herbaria in Europe, including the Natural His-tory Museum (BM), Royal Botanic Gardens, Kew (K),the Museum national d’Histoire naturelle (P), and theNaturhistorisches Museum Wien (W), is of particularimportance to Neotropical botany; these herbaria holdmany type specimens and collections by notable earlyexplorers of the Neotropics. In addition to stimulatingresearch, this increased investment in collections-basedresearch has spurred simultaneous growth and use of largedatabases of collections data and images, including iDig-Bio (,https://www.idigbio.org/.) and the Global Biodi-versity Information Facility (GBIF;,https://www.gbif.org/.).The Global Plants database (,https://plants.jstor.org/.)has made type images from around the globe availableonline; however, while its original intent was to empowerresearchers around the world (especially the Global South)with access to these important specimens, institutional feesnow make this a challenge.The recent emphasis on collections-based research

has resulted in a renaissance in biology (Funk, 2018).We have gained more in-depth understanding of phe-nology (Hart et al., 2014; Park et al., 2018), morpho-logical evolution (McAllister et al., 2018), the impacts ofclimate change on plant-animal interactions (Meineke& Davies, 2018), and shifting species ranges (Vellendet al., 2013). These advances would not have beenpossible without the depth of data through space andtime granted by collections. Improved molecular tech-niques have also allowed us to generate genome-scale

DNA sequence data (Hart et al., 2016), revolutionizingthe field of molecular systematics (Chomicki & Renner,2015; Iles et al., 2017; Dodsworth et al., 2019), atraditional realm of museum specimens. Further, theuse of degraded DNA from specimens has contributedto other biology subfields such as population genetics(Martin et al., 2016), local adaptation (Exposito-Alonsoet al., 2018), and microbiome ecology and evolution(Daru et al., 2018a).

Because of the increased interest in natural historycollections and their associated data, a more diversearray of scientists has been introduced to the innerworkings of museums than ever before. We hope thatthis has helped museums move away from a long-standing stereotype that taxonomists are misanthropeswho prefer to work in isolation. This is especially im-portant as it is likely that an even broader community ofend users of collections data will exist in the future(Schindel & Cook, 2018; Lendemer et al., 2020). It iscrucial to remember, though, that these creative, oftenbroad-scale studies that are being undertaken withincollections are only possible thanks to the massivecollecting efforts of the past. In particular, the resur-gence in floristic research in the 1970s through the early2000s led to major growth in Northern Hemisphereherbaria, as discussed below. These specimens, and thetaxonomists whose hard-earned specialist knowledgeaided the application of valid names, power most ofthe research conducted on the origin and maintenanceof Neotropical biodiversity today. While it is hearteningto see increased interest in natural history collections,their future utility hinges on the continued investment intaxonomy, which represents the foundation for high-quality biodiversity research (Wheeler, 2020).

CONTRIBUTIONS OF HISTORICAL COLLECTIONS TO OUR

MODERN UNDERSTANDING OF NEOTROPICAL BIODIVERSITY

Understanding the origin and maintenance of Neo-tropical biodiversity is difficult not only because of thecomplexity of the ecological and evolutionary processesthat generated these patterns, but also because of theenormous challenge of simply documenting and de-scribing diversity. Biodiversity documentation requiresfunding and the long-term dedication of teams of tax-onomists, knowledgeable field guides, artists, and pho-tographers. These efforts are not frequently undertaken;however, major events in the history of Neotropicalbotanical exploration, including significant expeditions,the development of institutions dedicated to the studyand preservation of biodiversity, floristic projects, andbotanical surveys, have shaped much of what we knowabout the Neotropical flora today.

Herbarium specimens are the medium through whichtaxonomic and systematic work is accomplished, and,

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with increased frequency, often form the basis of eco-logical and evolutionary studies. Much of the Neotropicsis under-collected relative to temperate regions, espe-cially given its high species diversity. We examined thedegree to which each Mesoamerican and South Amer-ican country has been botanically explored and docu-mented using the metric of vascular plant collectionsper land area (km2; Fig. 1). For comparison, we alsoincluded this metric for the United States and Spain.Costa Rica, by far, has the best-represented flora indigitized herbaria among all Latin American countries.This is undoubtedly due to a long history of botanicalexpeditions, institutional support, and flora projects inCosta Rica.To better understand how major events, including

floristic projects initiated by Missouri Botanical Gar-den, correlate with increases in herbarium collections,and, thus, our knowledge of the plant diversity in thoseareas, we assembled timelines of collection for selectedcountries in Central America (Nicaragua, Costa Rica,and Panama; Fig. 2) and South America (Venezuela,Colombia, and Ecuador; Fig. 3). Estimates of the num-ber of collections of vascular plants per year were takenfrom the number of preserved specimen occurrencesreported for Tracheophytes in GBIF. These timelineswere compared to major events in the history of botan-ical exploration for each country, which were confirmedfrom the literature (Nicaragua: Stevens et al., 2001;Montiel & Stevens, 2019; Costa Rica: Polakowsky,1879; Durand & Pittier, 1891; Durand et al., 1893;Tonduz, 1895; Pittier, 1908; Dodge, 1933; Standley,1937; Jimenez-Luthmer, 1969; Gomez & Savage, 1983;McCook, 1999; Leon, 2002; Hammel et al., 2004;Panama: Dwyer, 1964;Woodson& Schery, 1980; Moreno,2004; Venezuela: Huber & Wurdack, 1984; Berry et al.,1995; Colombia: Pinto & Ruiz, 1984; Forero, 1988;Callejas & Idarraga, 2013; Villamil-Montero & Ming,2016; Diazgranados et al., 2019; Ecuador: Diels, 1937;Acosta-Solis, 1969; Wiggins et al., 1971; Renner, 1993;Jørgensen & Leon-Yanez, 1999; and the MissouriBotanical Gardenwebsite:,http://www.mobot.org/MOBOT/Research/.).In each case, major expeditions, the establishment of

institutions (e.g., national herbaria, Instituto Nacionalde Biodiversidad [INBio] in Costa Rica, the Smithso-nian Tropical Research Institute [STRI] in Panama) andacademic programs (e.g., the Organization of TropicalStudies in Costa Rica), floristic projects, and ecologicalsurveys all had noticeable impacts on the number ofcollections made (Figs. 2, 3). These projects and insti-tutions have bolstered our knowledge and understand-ing of species numbers, distribution, composition, andcommunity assembly of the Neotropical flora as a whole.This understanding necessarily reflects known cul-

tural and logistic biases in biodiversity data (Hijmans

et al., 2000; Funk & Richardson, 2002; Meyer et al.,2016; Troudet et al., 2017; Daru et al., 2018b). Mostrelevant to the data presented above are temporal andcollector bias. For example, the time of year in whichcollectors tend to go to the field creates temporal bias innatural history records, which can extend into yearswhen collecting activity peaks or plummets (Funk &Morin, 2000; Norris et al., 2001). These bumper years, asdemonstrated by our timelines (Figs. 2, 3), often correlatewith specific projects or expeditions. This may introducecollector bias, and, in fact, the majority of collections inmany developing tropical countries result from few prolificcollectors, resulting in an overrepresentation of their pref-erences, including proclivities for specific taxa, habitattypes, or regions (Hijmans et al., 2000; Daru et al., 2018b).Cultural and logistic bias associated with the collection ofcertain taxa or clades over others leads to taxonomic andphylogenetic bias (Hortal et al., 2007). For example,arachnids, insects, and other invertebrates are underrep-resented in collections, while birds and angiosperms areoverrepresented, a trend that has increased over time(Troudet et al., 2017). Geographic bias, also known as“roadside bias,” refers to the higher density of collectionsmade in areas accessible by transportation, like roadsidesand riverbanks, and those surrounding major urban hubsand institutions, including herbaria andmuseums (Hijmanset al., 2000; Funk & Richardson, 2002; Loiselle et al.,2007). Additionally, each source of bias is accompa-nied by a level of taxonomic, geographic, and temporaluncertainty in the associated digitally accessible infor-mation. Biases and uncertainty limit the utility of broaderapplications (e.g., range maps and niche modeling) for theunderstanding of current biodiversity patterns, complicat-ing future biodiversity projections and the accurate doc-umentation of species composition and distribution patternsover time (Meyer et al., 2016; Troudet et al., 2017).Beyond an improved understanding of which and how

many species occur in the Neotropics, collectors havealso generated hypotheses about the processes under-lying biodiversity patterns. For example, during hisAndean expedition, Alexander von Humboldt noticedthat temperatures decreased as elevation increased,and, concomitantly, plant species changed (von Humboldt& Bonpland, 1807). From these observations, the hy-pothesis of altitudinal zonation was developed and re-mains a topic of investigation to this day (Snowden,1933; Johns, 1985; Ohsawa et al., 1985; Druitt et al.,1990; Frahm & Gradstein, 1991; Uhlig & Uhlig, 1991;Pendry & Proctor, 1996; Kessler, 2000; Sklenar, 2006).Similarly, Alwyn Gentry is perhaps best known for hislong-standing hypotheses regarding the origin andmaintenance of Neotropical floristic diversity, especiallyhow it relates to biogeography and landscape changethrough time (Gentry, 1982a, 1982b, 1988, 1992). Histaxonomic background (further discussed below) and

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abundant time spent making observations in the field in-spired his hypothesis that “Amazonian-centered” clades oflowland canopy trees and lianas have evolutionary historiesthat contrast with “Andean-centered” clades of mid- to high-elevation epiphytes, understory shrubs, or large monocots(Gentry, 1982a). This remains a major biogeographic hy-pothesis tested by systematists (Fleming et al., 1987; Clark,1990; Taylor, 1991; Cuesta-Camacho et al., 2006; Pirieet al., 2006; Quijano-Abril et al., 2006; Pennington &Dick,2010; Pinto et al., 2012; Lagomarsino et al., 2017), and hasbecome so ingrained in Neotropical botany that researchersoften present their study systems as “Amazonian-centered”(e.g., Macrolobium Schreb. section Macrolobium [(Murphyet al., 2018)], Swartzia Schreb. [Pinto et al., 2012]), or“Andean-centered” (e.g., Bambusoideae [Clark, 2001],Cen-tropogon C. Presl [Lagomarsino et al., 2016], Heliconia L.[Andersson, 1989]). Humboldt’s and Gentry’s contributionsexemplify how the powerful combination of taxonomic ex-pertise and extensive field observations can drive fields ofstudy for decades or centuries.

IN THE SPIRIT OF AL GENTRY: EXAMPLES OF INNOVATIVENEOTROPICAL BIODIVERSITY RESEARCH POWERED BY

TAXONOMIC KNOWLEDGE

Gentry’s hypotheses have stood the test of time andlaid the foundation for research into Neotropical floris-tics and biogeography that continues through today.

Gentry spent substantial time collecting plant speci-mens throughout the Neotropics, becoming acquaintedwith the taxonomic and morphological diversity of theflora. He was a consummate taxonomist, especially ofBignoniaceae, a group he worked on for his entire careerand for which he contributed treatments for numerousfloras (Miller et al., 1996). Gentry’s contributions to thestudy of Neotropical botany resulted directly from hisdeep taxonomic understanding of this focal group and itsplace within the broader context of Neotropical forests.Many of his insights came from establishing 226 tran-sects (now known as “Gentry plots”) in geographicallydistinct regions (Phillips & Miller, 2002), allowing himto consolidate his taxonomic and ecological data into aunified theory of Neotropical biogeography. Begun ini-tially as an avenue to understand the ecology of Bigno-niaceae (Miller et al., 1996), these plots transformedinto a key resource for the understanding of the taxo-nomic composition and overall patterns of plant diver-sity across tropical forests. Arguably, it is Gentry’straining and efforts as a taxonomist that allowed himto become not only one of the best tropical plant iden-tifiers who has ever lived, but also one of the mostimportant scientific thinkers of the 20th century.

Many researchers or groups of researchers haveadopted similar approaches to understanding theecology and evolution of Neotropical plants. Theseresearchers first develop taxonomic knowledge and

Figure 1. Number of vascular plant collections per land area (km2) for Mesoamerican and South American countries. Numberof collections for each country is based on the number of preserved specimen occurrences of Tracheophyta reported in GBIF(,https://www.gbif.org/.).

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resources for a particular group and, subsequently, usethat knowledge to test large-scale hypotheses in ecologyand evolution. Below, we highlight a few taxonomicgroups that complement Gentry’s approach to science,though it should be noted that many additional groupswould be equally well represented below. The prolifer-ation of model clades (Donoghue & Edwards, 2019) tostudy Neotropical biodiversity is likely thanks in largepart to the increased development of methods thatfacilitate analyses of biodiversity data (e.g., phyloge-netic comparative methods and species distributionmodels).

BIGNONIEAE (BIGNONIACEAE)

Al Gentry’s legacy of Bignoniaceae has been carriedforward, largely thanks to the contributions of LuciaLohmann’s group (Universidade de São Paulo, Brazil)in the tribe Bignonieae. Continued descriptions of newspecies (e.g., Firetti-Leggieri et al., 2015; Frazão &Lohmann, 2018), range extensions (e.g., Brito et al.,2018), checklists (e.g., Lohmann, 2010; Lohmann &Ulloa Ulloa, 2006), floristic treatments (e.g., Lohmannet al., 2018; Costa et al., 2019), synopses (e.g., Lohmann& Taylor, 2014; Fonseca & Lohmann, 2019), and mono-graphs (e.g., Medeiros & Lohmann, 2015; Francisco& Lohmann, 2018) are conducted in parallel withstudies on the phylogenetics (e.g., Lohmann, 2006;Kaehler et al., 2019), biogeography (e.g., Lohmann

et al., 2013; Thode et al., 2019), and evolution of traitsassociated with the climbing habit (e.g., Pace et al.,2011, 2015; Sousa-Baena et al., 2014), insect-plantinteractions (Nogueira et al., 2012, 2015), and pollina-tion systems (e.g., Alcantara & Lohmann, 2010, 2011),among others. Across these diverse works on Bignonia-ceae, an in-depth, organismally focused understandingof the ecology and evolution of the largest clade ofNeotropical lianas has emerged. As a result, the Bigno-niaceae represent as important a clade for understand-ing the origin and assembly of Neotropical biodiversityand biogeography today as they did when Gentry wasactive.

SOLANUM L. (SOLANACEAE)

Despite being one of the largest genera with ca.1500species, Solanum is an excellent example of how tax-onomic research can inform evolutionary research.Largely thanks to the leadership of Sandra Knapp(Natural History Museum) and Lynn Bohs (Universityof Utah), there is a large and vibrant community workingon various projects related to Solanum and the broaderSolanaceae. Taxonomic work in Solanum, includingmonographs, species descriptions, and floras, is incred-ibly active (e.g., Barboza, 2013; Stern et al., 2013;Sarkinen et al., 2015b; Knapp & Vorontsova, 2016;Sarkinen & Knapp, 2016; Knapp et al., 2019; Flora doBrasil, 2020). This is paired to frequent phylogenetic

Figure 2. Number of vascular plant collections per year with timelines of selected events for Nicaragua, Costa Rica, andPanama. Number of collections per year for each country were gathered from the number of preserved specimen occurrences ofTracheophyta reported in GBIF (,https://www.gbif.org/.) for each year. Events were confirmed from the literature (cited in maintext).

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updates (e.g., Weese & Bohs, 2007; Sarkinen et al.,2013a, 2015a; Spooner et al., 2018; Martine et al., 2019),including macroevolutionary studies (Echeverrıa-Londoñoet al., 2020). Thanks to this relatively complete (thoughcontinually updated) taxonomic knowledge, Solanum rep-resents an ideal clade in which to link genomics withvarious components of biodiversity (Knapp et al., 2004).In fact, Andean tomatoes are becoming a model system tounderstand evolutionary processes at play in rapid radi-ations (Baek et al., 2016; Pease et al., 2016; Hamlin &Moyle, 2019; Nevado et al., 2019). Insights from Solanumhave also played a major role in understanding speciesdistributions in the Neotropics (Knapp, 2002; Sarkinenet al., 2013b).

PROTIUM BURM F. (BURSERACEAE)

Protium is used as a model to study ecological andevolutionary dynamics of Amazonian trees (Daly et al.,2012), with an emphasis on edaphic specialization (Fineet al., 2004, 2005, 2013b). The ability to initially posequestions in Protium came from a solid foundation oftaxonomy, in recent years especially by Douglas Daly(New York Botanical Garden) (e.g., Daly, 1989, 1992,2007), complemented by a robust phylogenetic frame-work established by Paul Fine (University of California,Berkeley) (Fine et al., 2005, 2014). In turn, ecological

studies of habitat preferences coupled with new phylo-genetic data informed taxonomic revision (Daly & Fine,2011, 2018; Damasco et al., 2019; Daly, 2020) and themechanisms underlying habitat specialization and spe-ciation (Fine et al., 2013a, 2013b; Misiewicz & Fine,2014; Misiewicz et al., 2020). Additional research inProtium spans many subdisciplines of ecology and evo-lution (Zapata & Fine, 2013; Fortunel et al., 2016;Vleminckx et al., 2018), demonstrating the reach oftaxonomically centered research across subdisciplinesof biology.

CHALLENGES TO INCREASING THE REACH OF FLORISTICS AND

TAXONOMY

A major criticism of taxonomy is the field’s lack ofobjectivity (Turrill, 1957), a shortcoming that manysystematists acknowledge (Strasser, 2019). Respondingto this criticism, statistical methods have been devel-oped over the past few decades to make systematicsmore data-driven. Molecular systematics is a prime ex-ample: using variation in DNA sequences across species,phylogeneticists are able to apply biologically informedmodels to understand species relationships (e.g., Xi et al.,2012). Species delimitation methods are also catching upto the statistical rigor of phylogenetics, with model-basedmethods (e.g., Zapata & Jimenez, 2012; Yang, 2015)

Figure 3. Number of vascular plant collections per year with timelines of selected events for Venezuela, Colombia, andEcuador. Data collection was the same as in Figure 2.

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frequently applied instead of, or in addition to, a tax-onomic expert’s gestalt. This has resulted in a bloomingsubfield known as “integrative taxonomy” (Schlick-Steiner et al., 2010; Fujita et al., 2012; Prata et al.,2018), which reduces subjectivity and facilitates sta-bility in classification schemes. As a result, descriptivetaxonomy is becoming a more rigorous discipline(Sangster & Luksenberg, 2015). Monography, too, iscurrently in the midst of a 21st century revolution(Reginato, 2016; Zapata, 2018).An additional major impediment to extending floris-

tics and taxonomic research in recent decades has beenthe difficulty measuring its impact. While tools havebeen developed to quantify the reach of specimens,including Bionomia (Shorthouse & Page, 2019;,https://bionomia.net/.), there is a stigma about the limitedreach of museums and their curators. Furthermore,floras, monographs, and alpha taxonomic works arenot commonly cited, especially outside of the field ofsystematics (Werner, 2006; Wagele et al., 2011), evenwhen these works are the primary source of data forparticular research projects. This results in a reducedacademic profile for the researchers who conducttaxonomic research, impacting their career progres-sion. Indeed, hiring and promotion decisions, as wellas nominations for awards and fellowships, are madebased on metrics including citations (e.g., h-index,i-index) and other non-quantifiable dimensionsof “impact” that are not typically associated withherbarium-based researchers, all of which tend tobe lower for taxonomists. By devaluing taxonomy,academic culture can stymie the forward progressof the very basic cataloging and description of bio-diversity that is so critical for steady scientific progress ofall biodiversity-related research. Citing primary taxo-nomic literature whenever relevant is important to em-phasize fairly the importance of this branch of biology,while ensuring that research can be replicated.Finally, taxonomists need to do a better job inte-

grating with ecologists, evolutionary biologists, policymakers, and the general public. For example, conver-sation with policy makers, both domestic and interna-tional, is crucial to correctly and respectfully implementprotocols in the current complex ecosystem of regula-tions, including the Nagoya Protocol on Access andBenefit Sharing (Rabeler et al., 2019). Further, com-munication with diverse scientists can begin (or con-tinue) with the development of user-friendly floristictreatments and taxonomic tools, including identificationkeys and visual floras. Additionally, stability in taxon-omy should be a priority, to the extent that it is possiblein light of phylogenetic relationships. Taxonomic namechanges, especially to plants important in research or hor-ticulture, can cause particular uproar (Lowry et al., 2019),even when they follow taxonomic and nomenclatural best

practices (Nesom et al., 2019). In sum, systematists shouldbe considered just as important to answering the majorquestions of evolutionary biology, ecology, and conservationas experts from other subfields, and should be more com-monly integrated into efforts to understand global biodiver-sity patterns.

TOWARD AN INTEGRATED FUTURE WHERE MONOGRAPHY

AND FLORISTICS ARE AT THE CORE

No matter how complex a model or how large anassembled database is, there is no replacement fororganismal understanding, the realm of taxonomists.Inclusion of taxonomic experts in large-scale studiesof global diversity patterns is a crucial step towardintegrating monography and floristics and centeringstudy of the origin and maintenance of Neotropicalbiology in organismal biology and diversity. This isespecially important given the current emphasis onunderstanding tropical forest diversity and the subse-quent implications for conservation and the mitigationof climate change effects (Baker et al., 2017). As wecontinue to become increasingly interdisciplinary, it isessential that taxonomists are not only seen as a sourceof specimen identification, but, given their specialist’sperspective on organismal biology, also fully integratedinto research projects as key members of the team.Long-term ecological plots that add vouchered spec-

imen distribution information gained in a systematicway provide important insight into how the biodiversitycrisis is unfolding in diverse areas, both temperate andtropical. These plots are of huge value as they allow forfoundational research into tropical ecology, while con-tributing to the documentation of biodiversity (Condit,1995). They also present an opportunity to link taxon-omy to large-scale ecological studies. Given that a largeproportion of tropical plant species diversity is thoughtto be undescribed, continued vouchering of these plotsis likely to result in substantial species discovery. Infact, taxonomists have already begun to develop floras(Croat, 1978), describe new species and genera (van derWerff & Nishida, 2010; Kawasaki & Perez, 2012), andpublish identification guides (Muñoz et al., 2017) acrossthe many long-term forest plot sites. In turn, thesetaxonomic tools allow researchers to more accuratelyconduct their research, whether they are ecologistsdocumenting local processes governing community com-position or climate change scientists understandingpatterns of carbon sequestration.Despite the important contributions of forest plots to

biodiversity research, collections from plots presentbiases. For example, plots intended for long-term studyneed to be in areas where researchers can access the plotsrepeatedly, often in national parks and natural reserves.These protected areas likely provide a different picture of

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species composition than the disturbed areas that rep-resent the most common locations for general botanicalcollection (e.g., roadsides and pasture edges; Hijmanset al., 2000; Funk & Richardson, 2002; Loiselle et al.,2007). This results in amismatch between the habitats forwhich we have the most in-depth ecological knowledge(i.e., from established plots in forest interiors) and thosefrom which we understand the most about distribution,morphological variation, and taxonomy (i.e., roadsides).Further, sampling is typically restricted to woody plantsabove a certain diameter at breast height (DBH), andefforts to document herbaceous, lianescent, and epiphyticdiversity in long-term plots are much less common(Nieder et al., 2000; Kromer & Gradstein, 2003; Wolf& Alejandro, 2003; Flores-Palacios & Garcıa-Franco,2008; Obermuller et al., 2012; Campos et al., 2015), eventhough these plants make up a large portion of speciesdiversity, especially in Andean floras (Gentry, 1982a).Additionally, many specimens are sterile and thus, inaddition to being time-consuming to identify, are of limitedutility to taxonomists (Mori, 1992). We argue that, whilemaintaining long-term plots is essential to the study offorest dynamics through time and to the basic documen-tation of biodiversity, broader collection outside of thelimited number of plots is also essential.The continued collection of specimens in a system-

atic and replicable fashion is especially important asspecies distributions shift and species extinction riskincreases. An increased collection of vouchered plantdata requires the input and collaboration of taxonomicefforts, particularly if the resulting data are going to be ofmaximal utility to a broad user base (Baker et al., 2017).For example, large numbers of accurately identifiedspecimens are key to estimating accurate species dis-tributions (Feeley & Silman, 2011). In addition tocontinued collection, it is also important that taxono-mists continue to identify specimens in natural historycollections. Museum-based research is an importantsource for species discovery: ca. 50% of all speciesof plants that remain to be described are thought to havealready been collected and to be sitting in herbariawaiting to be discovered (Bebber et al., 2010). Unfor-tunately, given high levels of ecosystem destruction andbiodiversity loss, floras are increasingly becoming ahistorical record of what once existed, not what currentlyexists (Heywood, 2001). With this in mind, there is nomore important time to invest actively in the curationand growth of herbaria than the present. As May (1992)noted, there is a time limit to our discipline, and thistime may be approaching faster than we realize.Toward this end, it is crucial that governments and

institutions continue to support taxonomic research.This should not be hard to justify, given that fundingof taxonomically informed biodiversity studies in recentdecades has been very productive. For example, the

NSF Dimensions of Biodiversity grant program “As-sembly and evolution of the Amazonian biota and itsenvironment: An integrated approach” resulted not onlyin important breakthroughs related to understanding theorigin and maintenance of Amazonian biodiversitythrough novel fieldwork and extensive museum-basedresearch (e.g., Weeks et al., 2016; Nazareno et al.,2017; Bemmels et al., 2018; Fine & Lohmann, 2018;Cracraft et al., 2020), but also in important contributionsto a deeper understanding of the poorly known Ama-zonian geological history (e.g., Cheng et al., 2013;Wanget al., 2017; Pupim et al., 2019). Another importantexample of ongoing systematic collections efforts in theNeotropics is Kew’s Colombia Bio Program (,http://colplanta.org/.), which is actively conducting majorexpeditions to document plant and fungal flora of thisbiodiverse country, pairing these with original researchand product development, and working directly withColombian researchers to engender cultural changetoward greater awareness and appreciation of biodiver-sity by the general public and to provide actional rec-ommendations that will help Colombia become morecompetitive and sustainable in its use of biodiversity(Diazgranados et al., 2019). Importantly, these effortsexplicitly include Colombian researchers and partner-ships, including support from regional Colombian gov-ernments, as well as Kew and U.K. government bodies(see Acknowledging taxonomy’s colonial history below).

Continued investment in interdisciplinary work thatis centered around taxonomy, including emphasis onunder-studied taxa or regions, will result in a betterdescription of biodiversity and a more in-depth under-standing of ecological and evolutionary processes. Ul-timately, this support is key to mitigating the effects ofclimate change and developing conservation plans thatcan effectively reduce extinction risks of key species.Here, it is crucial that support be given to taxonomists sothey are able to summarize biodiversity data in com-prehensive monographs, develop well-researched floras,and infer the phylogenetic relationships that are socritical for stable classifications and a deeper under-standing of the evolutionary and biogeographical historyof biotas. Only by supporting curatorial efforts will weimprove our understanding of Neotropical plant diver-sity as a whole.

ACKNOWLEDGING TAXONOMY’S COLONIAL HISTORY

Finally, any call to revitalize taxonomy in the 21stcentury would be incomplete without mentioning theimportance of decolonizing the field. The history oftaxonomy, like allied fields including biogeography(Eichhorn et al., 2020) and field ecology (Baker et al.,2019), is rooted in colonial history. Harkening to thedays of Linnaeus, early history of modern taxonomy

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involved European explorers sponsored by imperialistgovernments bringing species native to colonial terri-tories back to Europe, where they received a Latin name(Heywood, 1983). Even today, though no longer explic-itly colonialist, European and North American taxono-mists still “discover” and name new tropical speciesthat have had traditional indigenous names for gener-ations (e.g., Whaanga et al., 2013). Further, taxonomicinfrastructure, including the number of registered taxon-omists and density of biodiversity collections, is under-represented in megadiverse countries of the GlobalSouth, including many in the Neotropics, even thoughthere are still disproportionate levels of biodiversity leftto describe in this region (Paknia et al., 2015; Barlowet al., 2018). To increase inclusivity and equity in tax-onomy, we must acknowledge this unequal access, con-front our painful history, and identify mechanisms inwhich to center, amplify, and support local perspectivesand integrate them into international efforts. A relativelyeasy first step (though we admit we do not take it here) isto identify and apply alternative terms to refer to thetropical region of the Western Hemisphere; the “NewWorld tropics,” “Neotropics,” and “American tropics”all reflect a colonizer perspective. Beyond changingcolonizer-centered terminology, researchers in theGlobal North should aim to build capacity in the LatinAmerican countries where they collect specimens anddescribe new taxa, include authors from those countriesin their research and publications, cite research prod-ucts produced exclusively by Latin American and in-digenous scholars, and explicitly include support forLatin American and indigenous researchers in fundingapplications where possible (Eichhorn et al., 2020).While taxonomy has historically been performed by

white researchers based in Northern Hemisphere insti-tutions, today’s ecosystem of Neotropical taxonomy isnotably international. This is likely partially due tonational and international regulation of biological ma-terial in which explicit collaboration with in-countryresearchers is a condition of approved research plans.However, we also observe many productive, connection-based collaborative relationships between researchersbased in Latin America and the Global North (includingones to which we belong). In order to explore the extentto which modern Neotropical taxonomy is a globalenterprise, we explored patterns of authorship in eightjournals with a focus on botanical taxonomy (i.e., Analesdel Real Jardın Botanico de Madrid, Brittonia, Calda-sia, Novon, Phytokeys, Phytotaxa, Systematic Botany,and Taxon). We first downloaded the full citation historyfor all papers including the Neotropics as a topic fromthese journals over the past decade (i.e., 2010–2020)from Web of Science (,http://webofscience.com/.).We then used the R package refsplitR (Fournieret al., 2020) to visualize collaborative networks of these

citations (Fig. 4B, C) using the primary institution thatan author is affiliated with as a proxy for their country.We subsequently visualized the total number of authorsbased in each country in the combined citations acrossall eight journals, scaled by each country’s estimatedpopulation, using rworldmap (South, 2011). Our resultssuggest that Latin American researchers are very activeparticipants in Neotropical plant taxonomy today (Fig.4) and that they are often part of international collab-orations, especially between researchers in the UnitedStates and western Europe (Fig. 4B, C). Some LatinAmerican countries (e.g., Brazil, Colombia, and CostaRica) have proportionally more active researchers pub-lishing on Neotropical taxonomy than the United States,while others do not have any representation in ourdataset (e.g., Paraguay, Nicaragua, and Surinam). Thesedifferences could be explained by lack of establishedinternational collaborative collection efforts (as notedabove), differences in national funding of scientificinfrastructure in the last decade (Ciocca & Delgado,2017), or differing academic publishing preferencesacross countries (Estrada-Mejıa & Forero-Pineda, 2010).We also observed differences in the structure of globalnetworks that reflect the scope and targeted audienceof different journals. For example, journals with anexplicit global focus (e.g., Phytotaxa) commonly havecollaboration networks that span multiple global re-gions, including both North America and western Europe(Fig. 4B), while regional journals (e.g., Caldasia) havenetworks centered in the country in which they arebased and tend to not extend to more than one regionof the Global North (Fig. 4C). Overall, these analysesdemonstrate that researchers based in Latin Americaactively publish on Neotropical plant taxonomy andform key components of international collaborative net-works. As decolonization efforts should be collaborative,community-accepted undertakings, any future progresstoward this end will benefit from the fact that LatinAmerican voices are already central to Neotropical planttaxonomy, as well as these existing international collab-orative networks.

POSITIONALITY STATEMENT

As white citizens of the United States who are trainedas scientists and employed by a major U.S. university,we recognize that we have a platform that is not availableto all taxonomists. In both of our careers, we haveworked throughout Latin America and in collaborationwith a variety of Latin American botanists, and haveimmensely benefitted from the diverse perspectives thatwe have encountered in the pursuit of scholarship inNeotropical taxonomy. So while we call for the field toreflect on the colonial history of the field, we alsorecognize that the present manuscript is an insignificant

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step toward realizing decolonization. Considerablescholarship, including by social scientists and historians,and input from a diversity of perspectives—especiallyLatin American and indigenous botanists—are essentialto effectively develop and communicate best practicesin the decolonialization of Neotropical plant taxonomy.

CONCLUSION

While we are not the first to note the importance oftaxonomy for richer biodiversity studies, we emphasizethe importance of making this connection clear so thatan increased appreciation for detailed understanding oforganismal diversity can be achieved. As the line be-tween the fields of taxonomy and evolutionary biologycontinues to blur, taxonomic experts increasingly usetheir organismal knowledge to understand importantpatterns and processes in ecology and evolution. Tax-onomists are integrated into expanded collaborativenetworks that aim to understand the drivers of biodi-versity patterns in key model systems, including Bigno-niaceae, Protium, and Solanum as discussed above, aswell as others featured in the 66th Missouri BotanicalGarden symposium such as the Andean lobelioids(Lagomarsino et al., 2017) and Psychotria (Sedioet al., 2013). Furthermore, taxonomic contributions arebeing published in high-profile, high-impact journalswith seemingly increased frequency (Hibbett, 2016;Cardoso et al., 2017; Muñoz-Rodrıguez et al., 2019;Rheindt et al., 2020). As we continue to move towardincreasingly integrated biodiversity studies, it is criticalthat taxonomists continue to bring their organismalknowledge to bear on broad questions related to theentire flora of the Neotropics, and that this is done in away that elevates voices and perspectives from Latin

American countries and indigenous cultures. It is alsocritical that entire research teams acknowledge the pastwork of botanists who built the knowledge base fromwhich they are able to generate and test broad hypoth-eses, as well as the broader historical context in whichthose taxonomists operated.

Literature Cited

Acosta-Solis, M. 1969. Proteccion y conservacion de la natural-eza en Sudamerica. Pp. 230–250 in E. J. Fittkau, J. Illies, H.Klinge, G. H. Schwabe & H. Sioli (editors), Biogeographyand Ecology in South America. Springer Netherlands,Dordrecht.

Akesson, C.M., F.Matthews-Bird, M. Bitting, C.-J. Fennell,W.B. Church, L. C. Peterson, B. G. Valencia, et al. 2020. 2,100years of human adaptation to climate change in the HighAndes. Nat. Ecol. Evol. 4: 66–74.

Alcantara, S. & L. G. Lohmann. 2010. Evolution of floralmorphology and pollination system in Bignonieae (Bigno-niaceae). Amer. J. Bot. 97: 782–796.

Alcantara, S. & L. G. Lohmann. 2011. Contrasting phyloge-netic signals and evolutionary rates in floral traits of Neo-tropical lianas. Biol. J. Linn. Soc. 102: 378–390.

Andersson, L. 1989. An evolutionary scenario for the genusHeliconia. Pp. 173–184 in L. B. Holmnielsen, I. C. Nielsen& H. Balsev (editors), Tropical Forest: Botanical Dynamics,Speciation and Diversity. Academic Press, London.

Antonelli, A. & I. Sanmartın. 2011. Why are there so manyplant species in the Neotropics? Taxon 60: 403–414.

Antonelli, A., M. Ariza, J. Albert, T. Andermann, J. Azevedo,C. Bacon, S. Faurby, et al. 2017. Conceptual and empiricaladvances in Neotropical biodiversity research. PeerJ Prepr.6: e5644.

Bacon, C. D., D. Silvestro, C. Jaramillo, B. T. Smith, P.Chakrabarty & A. Antonelli. 2015. Biological evidencesupports an early and complex emergence of the Isthmusof Panama. Proc. Natl. Acad. Sci. U.S.A. 112: 6110–6115.

Baek, Y. S., S. M. Royer, A. K. Broz, P. A. Covey, G. Lopez-Casado, R. Nuñez, P. J. Kear, et al. 2016. Interspecificreproductive barriers between sympatric populations of wild

Figure 4. Distribution and networks of authors publishing on Neotropical taxonomy. —A. Global distribution of authors’institutions on Neotropical botany taxonomic publications from eight targeted journals from a Web of Science search, scaled byestimated population of each country. Colors represent number of authors per million on a sliding scale from light gray to black;there were no authors in our dataset from countries in white.—B. Author networks for one journal with an explicitly global reach(Phytotaxa). —C. Author networks for one journal with an explicitly local reach (Caldasia, a Colombian journal).

Volume 105, Number 32020

Lagomarsino & FrostTaxonomy in the Study of NeotropicalBiodiversity

415

tomato species (Solanum section Lycopersicon). Amer. J. Bot.103: 1964–1978.

Baker, K., M. P. Eichhorn & M. Griffiths. 2019. Decolonizingfield ecology. Biotropica 51: 288–292.

Baker, T. R., R. T. Pennington, K. G. Dexter, P. V. A. Fine, H.Fortune-Hopkins, E. N. Honorio, I. Huamantupa-Chuquimaco,et al. 2017. Maximising synergy among tropical plant sys-tematists, ecologists, and evolutionary biologists. Trends Ecol.Evol. 32: 258–267.

Barboza, G. E. 2013. In F. Zuloaga, M. Belgrano & A. Anton(editors), Flora Vascular de la Republica Argentina 13:Dicotyledoneae-Solanaceae. Instituto de Botanica Darwin-ion, San Isidro.

Barlow, J., F. França, T. A. Gardner, C. C. Hicks, G. D. Lennox,E. Berenguer, L. Castello, et al. 2018. The future of hyper-diverse tropical ecosystems. Nature 559: 517–526.

Basset, Y., V. Novotny, S. E. Miller, G. D.Weiblen, O. Missa &A. J. A. Stewart. 2004. Conservation and biological moni-toring of tropical forests: The role of parataxonomists.J. Appl. Ecol. 41: 163–174.

Bebber, D. P., M. A. Carine, J. R. I. Wood, A. H. Wortley, D. J.Harris, G. T. Prance, G. Davidse, et al. 2010. Herbaria are amajor frontier for species discovery. Proc. Natl. Acad. Sci.U.S.A. 107: 22169–22171.

Bebber, D. P., J. R. I.Wood, C. Barker &R.W. Scotland. 2014.Author inflation masks global capacity for species discoveryin flowering plants. New Phytol. 201: 700–706.

Bemmels, J. B., S. J. Wright, N. C. Garwood, S. A. Queen-borough, R. Valencia & C. W. Dick. 2018. Filter-dispersalassembly of lowland Neotropical rainforests across theAndes. Ecography 41: 1763–1775.

Berry, P. E., B. K. Holst & K. Yatskievych. 1995. Flora of theVenezuelan Guayana, Vol. 1. Missouri Botanical GardenPress, St. Louis; Timber Press, Portland.

Brito, I. J. N., S. L. Costa, J. M. P. Cordeiro, L. G. Lohmann &J. I. M. de Melo. 2018. New records of the Tabebuia alliance(Bignoniaceae) for the state of Paraiba, northeastern Brazil.Rev. Mex. Biodivers. 89: 625–630.

Buyck, B. 1999. Taxonomists are an endangered species inEurope. Nature 401: 321.

Callejas, R. & A. Idarraga. 2013. Flora de Antioquia: Catalogo de lasPlantas Vasculares. Vol. I. Introduccion. Editorial D’Vinni, Bogota.

Campos, L. V., H. ter Steege & J. Uribe. 2015. The epiphyticbryophyte flora of the Colombian Amazon. Caldasia 37: 47–59.

Cardoso, D., T. Sarkinen, S. Alexander, A. M. Amorim, V.Bittrich, M. Celis, D. C. Daly, et al. 2017. Amazon plantdiversity revealed by a taxonomically verified species list.Proc. Natl. Acad. Sci. U.S.A. 114: 10695–10700.

Cardoso, P., T. L. Erwin, P. A. V. Borges & T. R. New. 2011.The seven impediments in invertebrate conservation andhow to overcome them. Biol. Conserv. 144: 2647–2655.

Cheng, H., A. Sinha, F. W. Cruz, X. Wang, R. L. Edwards, F.M. d’Horta, C. C. Ribas, et al. 2013. Climate change patternsin Amazonia and biodiversity. Nat. Commun. 4: 1411.

Chomicki, G. & S. S. Renner. 2015. Watermelon origin solvedwith molecular phylogenetics including Linnaean material:Another example of museomics. New Phytol. 205: 526–532.

Ciocca, D. R. & G. Delgado. 2017. The reality of scientificresearch in Latin America; an insider’s perspective. CellStress Chaperones 22: 847–852.

Claramunt, S. & J. Cracraft. 2015. A new time tree revealsEarth history’s imprint on the evolution of modern birds. Sci.Adv. 1: e1501005.

Clark, L. G. 1990. Chusquea sect. Longiprophyllae (Poaceae:Bambusoideae): A new Andean section and new species.Syst. Bot. 15: 617–634.

Clark, L. G. 2001. Diversification and endemism in Andeanwoody bamboos (Poaceae: Bambusoideae). J. Amer. BambooSoc. 15: 14–19.

Condit, R. 1995. Research in large, long-term tropical forestplots. Trends Ecol. Evol. 10: 18–22.

Costa, S., L. G. Lohmann & M. T. Buril. 2019. Flora ofPernambuco, Brazil: Tabebuia alliance and tribe Jacaran-deae (Bignoniaceae). Biota Neotrop. 19: e20190737. https://doi.org/10.1590/1676-0611-bn-2019-0737.

Cracraft, J., C. C. Ribas, F. M. d’Horta, J. Bates, R. P. Almeida,P. Baker, J. P. Boubli, et al. 2020. The origin and evolution ofAmazonian species diversity. Pp. 225–244 in V. Rull & A.Carnaval (editors), Neotropical Diversification: Patterns andProcesses. Springer, Berlin.

Croat, T. B. 1978. Flora of Barro Colorado Island. StanfordUniversity Press, Stanford.

Cuesta-Camacho, F., A. Ganzenmueller & F. Baquero. 2006.Predicting distribution of Andean-centered taxa using eco-logical niche modelling methods. Lyonia 9: 19–33.

Daly,D.C. 1989. Studies inNeotropical Burseraceae. II. Genericlimits in New World Protieae and Canarieae. Brittonia 41:17–27.

Daly, D. C. 1992. New taxa and combinations inProtiumBurm.f. Studies in Neotropical Burseraceae VI. Brittonia 44: 280.

Daly, D. C. 2007. A new section of Protium from the Neotropics.Studies in Neotropical Burseraceae XIII. Brittonia 59: 1–24.

Daly, D. C. 2020. New species of Protium sect. Tetragastrisfrom the Andes, the Brazilian Cerrado, and Amazonia.Studies in Neotropical Burseraceae XXVIII. Brittonia.doi:10.1007/s12228-020-09616-x.

Daly, D. C. & P. V. A. Fine. 2011. A new Amazonian sectionof Protium (Burseraceae) including both edaphic specialistand generalist taxa. Studies in Neotropical BurseraceaeXVI. Syst. Bot. 36: 939–949.

Daly, D. C. & P. V. A. Fine. 2018. Generic limits re-visited andan updated sectional classification for Protium (tribe Pro-tieae). Studies in Neotropical Burseraceae XXV. Brittonia70: 418–426.

Daly, D. C., P. V. A. Fine & M. C. Martınez-Habibe. 2012.Burseraceae: A model for studying the Amazon flora. Rodri-guesia 63: 021–030.

Damasco, G., D. C. Daly, A. Vicentini & P. V. A. Fine. 2019.Reestablishment of Protium cordatum (Burseraceae) basedon integrative taxonomy. Taxon 68: 34–46.

Daru, B. H., E. A. Bowman, D. H. Pfister & A. E. Arnold.2018a. A novel proof of concept for capturing the diversity ofendophytic fungi preserved in herbarium specimens. Philos.Trans., Ser. B 374: 20170395. doi:10.1098/rstb.2017.0395.

Daru, B. H., D. S. Park, R. B. Primack, C. G. Willis, D. S.Barrington, T. J. S. Whitfeld, T. G. Seidler, et al. 2018b.Widespread sampling biases in herbaria revealed fromlarge-scale digitization. New Phytol. 217: 939–955.

Diaz, L. F. H., L. J. Harmon, M. T. C. Sugawara, E. T. Miller& M. W. Pennell. 2019. Macroevolutionary diversificationrates show time dependency. Proc. Natl. Acad. Sci. U.S.A.116: 7403–7408.

Diazgranados, M., F. Avila, M. Alvarez, E. Ambrose, D. Baines,A. Barker, D. Bishop, et al. 2019. ColPlantA: Colombianresources for Plants made Accessible. Royal Botanic Gar-dens, Kew. ,http://colplanta.org..

Dick, C. W. & M. Heuertz. 2008. The complex biogeographichistory of a widespread tropical tree species. Evolution 62:2760–2774.

Diels, L. 1937. Beitrage zur Kenntnis der Vegetation und Floravon Ecuador. Biblioteca Botanica, Stuttgart.

Dodge, C. W. 1933. The foliose and fruticose lichens of CostaRica. I. Ann. Missouri Bot. Gard. 20: 373–467.

416 Annals of theMissouri Botanical Garden

Dodsworth, S., L. Pokorny, M. G. Johnson, J. T. Kim, O.Maurin, N. J. Wickett, F. Forest, et al. 2019. Hyb-seq forflowering plant systematics. Trends Pl. Sci. 24: 887–891.

Donoghue, M. J. & E. J. Edwards. 2019. Model clades are vitalfor comparative biology, and ascertainment bias is not aproblem in practice: A response to Beaulieu and O’Meara(2018). Amer. J. Bot. 106: 327–330.

Druitt, D. G., N. J. Enright & J. Ogden. 1990. Altitudinalzonation in the mountain forests of Mt Hauhungatahi, NorthIsland, New Zealand. J. Biogeogr. 17: 205–220.

Durand, T. & H. Pittier. 1891. Primitiae florae costaricensis.Bull. Soc. Roy. Bot. Belgique 30: 7–97.

Durand, T., H. Pittier, J. Muller, F. Renauld & J. Cardot. 1893.Primitiae florae costaricensis, troisieme fascicule. Bull. Soc.Roy. Bot. Belgique 32: 122–201.

Dwyer, J. D. 1964. Panama, plant collection, and the MissouriBotanical Garden. Ann. Missouri Bot. Gard. 51: 109–117.

Echeverrıa-Londoño, S., T. Sarkinen, I. S. Fenton, A. Purvis &S. Knapp. 2020. Dynamism and context-dependency indiversification of the megadiverse plant genus Solanum(Solanaceae). J. Syst. Evol. doi:10.1111/jse.12638.

Eck, J. L., S. M. Stump, C. S. Delavaux, S. A. Mangan & L. S.Comita. 2019. Evidence of within-species specialization bysoil microbes and the implications for plant communitydiversity. Proc. Natl. Acad. Sci. U.S.A. 116: 7371–7376.

Eichhorn, M. P., K. Baker & M. Griffiths. 2020. Steps towarddecolonising biogeography. Frontiers Biogeogr. 12: e44795.

Estrada-Mejıa, C. & C. Forero-Pineda. 2010. The quest forvisibility of scientific journals in Latin America. Learn.Publ. 23: 237–252.

Exposito-Alonso, M., C. Becker, V. J. Schuenemann, E. Reiter,C. Setzer, R. Slovak, B. Brachi, et al. 2018. The rate andpotential relevance of new mutations in a colonizing plantlineage. PLoS Genet. 14: e1007155.

Feeley, K. J. & M. R. Silman. 2011. Keep collecting: Accuratespecies distribution modelling requires more collectionsthan previously thought. Divers. Distrib. 17: 1132–1140.

Fine, P. V. A. & L. G. Lohmann. 2018. Importance of dispersalin the assembly of the Neotropical biota. Proc. Natl. Acad.Sci. U.S.A. 115: 5829–5831.

Fine P. V. A., I. Mesones & P. D. Coley. 2004. Herbivorespromote habitat specialization by trees in Amazonian forests.Science 305: 663–665.

Fine, P. V. A., D. C. Daly & K. M. Cameron. 2005. Thecontribution of edaphic heterogeneity to the evolution anddiversity of Burseraceae trees in the western Amazon. Evo-lution 59: 1464–1478.

Fine, P. V. A., M. R. Metz, J. Lokvam, I. Mesones, J. M. AyarzaZuñig, G. P. A. Lamarre, M. Vasquez Pilco, et al. 2013a. Insectherbivores, chemical innovation and the evolution of habitatspecialization in Amazonian trees. Ecology 94: 1764–1775.

Fine, P. V. A., F. Zapata, D. C. Daly, I. Mesones, T. M.Misiewicz, H. F. Cooper & C. E. A. Barbosa. 2013b. Theimportance of environmental heterogeneity and spatial dis-tance in generating phylogeographic structure in edaphicspecialist and generalist tree species of Protium (Burser-aceae) across the Amazon Basin. J. Biogeogr. 40: 646–661.

Fine, P. V. A., F. Zapata & D. C. Daly. 2014. Investigatingprocesses of neotropical rain forest tree diversification byexamining the evolution and historical biogeography of theProtieae (Burseraceae). Evolution 68: 1988–2004.

Firetti-Leggieri, F., D. Demarco & L. G. Lohmann. 2015. Anew species of Anemopaegma (Bignonieae, Bignoniaceae)from the Atlantic Forest of Brazil. Phytotaxa 219: 174–182.

Fleming, T. H., R. Breitwisch & G. H. Whitesides. 1987.Patterns of tropical vertebrate frugivore diversity. AnnualRev. Ecol. Syst. 18: 91–109.

Flora do Brasil. 2020 (under construction). Jardim Botanico doRio de Janeiro. ,http://floradobrasil.jbrj.gov.br/., accessedon 1 July 2020.

Flores-Palacios, A. & J. G. Garcıa-Franco. 2008. Habitatisolation changes the beta diversity of the vascular epiphytecommunity in lower montane forest, Veracruz, Mexico.Biodivers. & Conservation 17: 191–207.

Fonseca, L. H. M. & L. G. Lohmann. 2019. An updatedsynopsis of Adenocalymma (Bignonieae, Bignoniaceae).Syst. Bot. 44: 893–912.

Forero, E. 1988. Botanical exploration and phytogeography ofColombia: Past, present and future. Taxon 37: 561–566.

Fortunel, C., C. E. T. Paine, P. V. A. Fine, I. Mesones, J.-Y.Goret, B. Burban, J. Cazal, et al. 2016. There’s no place likehome: Seedling mortality contributes to the habitat special-isation of tree species across Amazonia. Ecol. Lett. 19: 1256–1266.

Fournier, A. M., M. E. Boone, F. R. Stevens & E. M. Bruna.2020. refsplitr: Author name disambiguation, author geore-ferencing, and mapping of coauthorship networks with Webof Science data. J. Open Source Softw. 5: 2028.

Frahm, J.-P. & S. R. Gradstein. 1991. An altitudinal zonationof tropical rain forests using byrophytes. J. Biogeogr. 18:669–678.

Francisco, J. N. C. & L. G. Lohmann. 2018. Taxonomic revisionof Pachyptera (Bignonieae, Bignoniaceae). Phytotaxa 92:89–131.

Frazão, A. & L. G. Lohmann. 2018. A new species of Tanae-cium (Bignonieae, Bignoniaceae) from the Brazilian Amazonand its phylogenetic placement. Pl. Syst. Evol. 304:1245–1253.

Fujita, M. K., A. D. Leache, F. T. Burbrink, J. A. McGuire & C.Moritz. 2012. Coalescent-based species delimitation in anintegrative taxonomy. Trends Ecol. Evol. 27: 480–488.

Funk, V. A. 2018. Collections-based science in the 21stcentury. J. Syst. Evol. 56: 175–193.

Funk, V. A. & N. Morin. 2000. A survey of the herbaria of thesoutheast United States. Sida Bot. Misc. 18: 35–52.

Funk, V. A. & K. S. Richardson. 2002. Systematic data inbiodiversity studies: Use it or lose it. Syst. Biol. 51: 303–316.

Gaston, K. J. & R. M. May. 1992. Taxonomy of taxonomists.Nature 356: 281–282.

Gentry, A. H. 1982a. Neotropical floristic diversity: Phytogeo-graphical connections between Central and South America,Pleistocene climatic fluctuations, or an accident of theAndean orogeny? Ann. Missouri Bot. Gard. 69: 557–593.

Gentry, A. H. 1982b. Patterns of Neotropical plant speciesdiversity. Pp. 1–84 in M. K. Hecht, B. Wallace & G. T.Prance (editors), Evolutionary Biology, Vol. 15. Springer,Boston.

Gentry, A. H. 1988. Changes in plant community diversity andfloristic composition on environmental and geographicalgradients. Ann. Missouri Bot. Gard. 75: 1–34.

Gentry, A. H. 1992. Tropical forest biodiversity: Distributionalpatterns and their conservational significance. Oikos 63:19–28.

Gomez, L. D. & J. M. Savage. 1983. Searchers on that richcoast: Costa Rican field biology, 1400–1980. Pp. 1–11 inD. H. Janzen (editor), Costa Rican Natural History. Univer-sity of Chicago Press, Chicago.

Goodwin, Z. A., D. J. Harris, D. Filer, J. R. I. Wood & R. W.Scotland. 2015. Widespread mistaken identity in tropicalplant collections. Curr. Biol. 25: R1066–R1067.

Hamlin, J. A. P. & L. C. Moyle. 2019. Spatial proximitydetermines post-speciation introgression in Solanum. bio-Rxiv. https://doi.org/10.1101/529115.

Volume 105, Number 32020

Lagomarsino & FrostTaxonomy in the Study of NeotropicalBiodiversity

417

Hammel, B. E., M. H. Grayum, C. Herrera & N. Zamora(editors). 2004. Manual de Plantas de Costa Rica, Vol. I:Introduccion. Monogr. Syst. Bot. Missouri Bot. Gard. 97.

Hart, M. L., L. L. Forrest, J. A. Nicholls & C. A. Kidner. 2016.Retrieval of hundreds of nuclear loci from herbarium spec-imens. Taxon 65: 1081–1092.

Hart, R., J. Salick, S. Ranjitkar & J. Xu. 2014. Herbariumspecimens show contrasting phenological responses to Hima-layan climate. Proc. Natl. Acad. Sci. U.S.A. 111: 10615–10619.

Hawkins, B. A. 2001. Ecology’s oldest pattern? Trends Ecol.Evol. 16: 470.

Heywood, V. H. 1983. The mythology of taxonomy. Trans. Bot.Soc. Edinburgh 44: 79–94.

Heywood, V. 2001. Floristics and monography—An uncertainfuture? Taxon 50: 361–380.

Hibbett, D. 2016. The invisible dimension of fungal diversity.Science 351: 1150–1151.

Hijmans, R. J., K. A. Garrett, Z. Huaman, D. P. Zhang, M.Schreuder &M. Bonierbale. 2000. Assessing the geographicrepresentativeness of genebank collections: The case ofBolivian wild potatoes. Conserv. Biol. 14: 1755–1765.

Hinchliff, C. E., S. A. Smith, J. F. Allman, J. G. Burleigh, R.Chaudhary, L. M. Coghill, K. A. Crandall, et al. 2015.Synthesis of phylogeny and taxonomy into a comprehensivetree of life. Proc. Natl. Acad. Sci. U.S.A. 112: 12764–12769.

Hoorn, C., R. van der Ham, F. de la Parra, S. Salamanca, H. terSteege, H. Banks, W. Star, et al. 2019. Going north andsouth: The biogeographic history of two Malvaceae in thewake of Neogene Andean uplift and connectivity betweenthe Americas. Rev. Palaeobot. Palynol. 264: 90–109.

Hortal, J., A. Jimenez-Valverde, J. F. Gomez, J. M. Lobo & A.Baselga. 2008. Historical bias in biodiversity inventoriesaffects the observed environmental niche of the species.Oikos 117: 847–858.

Huber, O. & J. J. Wurdack. 1984. History of botanical explo-ration in Territorio Federal Amazonas, Venezuela. Smithso-nian Contrib. Bot. 56: 1–83.

Iles, W. J. D., C. Sass, L. Lagomarsino, G. Benson-Martin, H.Driscoll & C. D. Specht. 2017. The phylogeny of Heliconia(Heliconiaceae) and the evolution of floral presentation.Molec. Phylogen. Evol. 117: 150–167.

Jimenez-Luthmer, O. 1969. La influencia de Humboldt en lacultura de Costa Rica. Rev. Agric. (Piracicaba) 61: 10–11.

Johns, R. J. 1985. Altitudinal zonation of pteridophytes inPapuasia. Proc. Roy. Soc. Edinburgh 86: 381–389.

Jørgensen, P. M. & S. Leon-Yanez. 1999. Catalogue of the VascularPlants of Ecuador. Monogr. Syst. Bot. Missouri Bot. Gard. 75.

Kaehler, M., F. A. Michelangeli & L. G. Lohmann. 2019. Fine-tuning the circumscription of Fridericia (Bignonieae, Bigno-niaceae). Taxon 68: 751–770.

Kawasaki, M. L. & A. J. Perez. 2012. A new species of Plinia(Myrtaceae) from Ecuador, with demographic notes from alarge forest plot. Harvard Pap. Bot. 17: 19–20.

Kessler, M. 2000. Altitudinal zonation of Andean cryptogamcommunities. J. Biogeogr. 27: 275–282.

Knapp, S. 2002. Assessing patterns of plant endemism inNeotropical uplands. Bot. Rev. 68: 22–37.

Knapp, S. &M. S. Vorontsova. 2016. A revision of the “AfricanNon-Spiny” Clade of Solanum L. (Solanum sections Afro-solanum Bitter, Benderianum Bitter, Lemurisolanum Bitter,Lyciosolanum Bitter, Macronesiotes Bitter, and Quadrangu-lare Bitter: Solanaceae). PhytoKeys 66: 1–142.

Knapp, S., L. Bohs, M. Nee & D. M. Spooner. 2004. Sol-anaceae—A model for linking genomics with biodiversity.Int. J. Genomics Proteomics 5: 285–291.

Knapp, S., G. E. Barboza, L. Bohs & T. Sarkinen. 2019. Arevision of the Morelloid Clade of Solanum L. (Solanaceae)

in North and Central America and the Caribbean. PhytoKeys123: 1–144.

Kromer, T. & S. R. Gradstein. 2003. Species richness ofvascular epiphytes in two primary forests and fallows inthe Bolivian Andes. Selbyana 24: 190–195.

Lagomarsino, L. P., F. L. Condamine, A. Antonelli, A. Mulch&C. C. Davis. 2016. The abiotic and biotic drivers of rapiddiversification in Andean bellflowers (Campanulaceae).New Phytol. 210: 1430–1442.

Lagomarsino, L. P., E. J. Forrestel, N. Muchhala & C. C. Davis.2017. Repeated evolution of vertebrate pollination syn-dromes in a recently diverged Andean plant clade. Evolution71: 1970–1985.

Lendemer, J., B. Thiers, A. K. Monfils, J. Zaspel, E. R. Ellwood,A. Bentley, K. LeVan, et al. 2020. The Extended SpecimenNetwork: A strategy to enhance US biodiversity collections,promote research and education. BioScience 70: 23–30.

Leon, J. 2002. La exploracion botanica de Costa Rica en elsiglo XIX. Pp. 161–178 in G. Peraldo Huertas (editor),Ciencia y Tecnica en la Costa Rica del Siglo XIX. EditorialTecnologica de Costa Rica, Cartago.

Lohmann, L. G. 2006. Untangling the phylogeny of neotropicallianas (Bignonieae, Bignoniaceae). Amer. J. Bot. 93: 304–318.

Lohmann, L. G. 2010. Bignoniaceae. Pp. 758–772 in R. C.Forzza, J. F. A. Baumgartz, C. E. M. Bicudo, A. A. CarvalhoJr., A. Costa, D. P. Costa, M. Hopkins, et al. (editors),Catalogo de Plantas e Fungos do Brasil. Jardim Botanicodo Rio de Janeiro, Rio de Janeiro.

Lohmann, L. G. & C. Ulloa Ulloa. 2006. Bignoniaceae. iPlantsprototype Checklist. New York Botanical Garden, MissouriBotanical Garden, Royal Botanic Gardens, Kew. ,http://www.iplants.org/..

Lohmann, L. G. & C. M. Taylor. 2014. A new generic clas-sification of tribe Bignonieae (Bignoniaceae). Ann. MissouriBot. Gard. 99: 348–489.

Lohmann, L. G., C. D. Bell, M. F. Calio & R. C. Winkworth.2013. Pattern and timing of biogeographical history in theNeotropical tribe Bignonieae (Bignoniaceae). Bot. J. Linn.Soc. 171: 154–170.

Lohmann, L. G., F. Firetti & B. Gomes. 2018. Flora rupestredas cangas da Serra dos Carajas: Bignoniaceae. Rodriguesia69: 1063–1079.

Loiselle, B. A., P. M. Jørgensen, T. Consiglio, I. Jimenez, J. G.Blake, L. G. Lohmann & O. M. Montiel. 2007. Predictingspecies distributions from herbarium collections: Does cli-mate bias in collection sampling influence model outcomes?J. Biogeogr. 35: 105–116.

Lowry, D. B., J. M. Sobel, A. L. Angert, T. Ashman, R. L. Baker,B. K. Blackman, Y. Brandvain, et al. 2019. The case for thecontinued use of the genus name Mimulus for all monkey-flowers. Taxon 68: 617–623.

Maldonado, C., C. I. Molina, A. Zizka, C. Persson, C. M. Taylor,J. Alban, E. Chilquillo, et al. 2015. Estimating speciesdiversity and distribution in the era of Big Data: To whatextent can we trust public databases? Global Ecol. Biogeogr.24: 973–984.

Martin, M. D., M. T. Olsen, J. A. Samaniego, E. A. Zimmer& M. T. P. Gilbert. 2016. The population genomic basis ofgeographic differentiation in North American common rag-weed (Ambrosia artemisiifolia L.). Ecol. Evol. 6: 3760–3771.

Martine, C. T., I. E. Jordon-Thaden, A. J. McDonnell, J. T.Cantley, D. S. Hayes, M. D. Roche, E. S. Frawley, et al.2019. Phylogeny of the Australian Solanum dioicumgroup using seven nuclear genes, with considerationof Symon’s fruit and seed dispersal hypotheses. PLoSONE 14: e0207564.

418 Annals of theMissouri Botanical Garden

May, R. M. 1992. How many species inhabit the Earth? Sci.Amer. 267: 42–49.

McAllister, C. A., M. R. McKain, M. Li, B. Bookout & E. A.Kellogg. 2018. Specimen-based analysis of morphology andthe environment in ecologically dominant grasses: The powerof the herbarium. Philos. Trans., Ser. B 374: 20170403.

McCook, S. 1999. Creole science: Botanical surveys of CostaRica, 1880–1940. Endeavour 23: 118–120.

Medeiros, M. C. P. & L. G. Lohmann. 2015. Taxonomicrevision of Tynanthus (Bignonieae, Bignoniaceae). Phyto-taxa 216: 1–60.

Meineke, E. K. & T. J. Davies. 2018. Museum specimensprovide novel insights into changing plant-herbivore inter-actions. Philos. Trans., Ser. B 374: 20170393.

Meyer, C., P. Weigelt & H. Kreft. 2016. Multidimensionalbiases, gaps and uncertainties in global plant occurrenceinformation. Ecol. Lett. 19: 992–1006.

Miller, J. S., T. M. Barkley, H. H. Iltis, W. H. Lewis, E. Forero,M. Plotkin, O. Phillips, et al. 1996. Alwyn Howard Gentry,1945–1993: A tribute. Ann. Missouri Bot. Gard. 83: 433–460.

Miralles, A., T. Bruy, K. Wolcott, M. D. Scherz, D. Begerow, B.Beszteri, M. Bonkowski, et al. 2020. Repositories for tax-onomic data: Where we are and what is missing. Syst. Biol.doi:10.1093/sysbio/syaa026.

Misiewicz, T. M. & P. V. A. Fine. 2014. Evidence for ecologicaldivergence across a mosaic of soil types in an Amazoniantropical tree: Protium subserratum (Burseraceae). Molec.Ecol. 23: 2543–2558.

Misiewicz, T. M., T. Simmons & P. V. A. Fine. 2020. Thecontribution of multiple barriers to reproduction betweenedaphically divergent lineages in the Amazonian tree Pro-tium subserratum (Burseraceae). Ecol. Evol. 10: 6646–6663.

Montiel, O. M. & W. D. Stevens. 2019. Botanical studies inNicaragua: An ongoing journey of 50-plus years. ReVista.19: 1–4.

Moreno, S. H. 2004. Naturalists on the Isthmus of Panama: AHundredYears of Natural History on the Biological Bridge ofthe Americas. Smithsonian Tropical Research Institute,Panama.

Mori, S. A. 1992. Neotropical floristics and inventory: Who willdo the work? Brittonia 44: 372–375.

Muñoz, G. V., N. C. Garwood, M. S. Bass & H. Navarette, withthe Huaorani communities of Guiyero, Timpoca and Dicaro.2017. The Common Trees of Yasunı: A Guide for Identifyingthe Common Trees of the Ecuadorian Amazon. FindingSpecies, Inc., Quito (with Pontifica Universidad Catolicadel Ecuador, Darwin Initiative, and Natural History Mu-seum, London).

Muñoz-Rodrıguez, P., T. Carruthers, J. R. I. Wood, B. R. M.Williams, K. Weitemier, B. Kronmiller, Z. Goodwin, et al.2019. A taxonomic monograph of Ipomoea integrated acrossphylogenetic scales. Nat. Plants 5: 1136–1144.

Murphy, B., M. de la Estrella, R. Schley, F. Forest &B. Klitgard. 2018. On the monophyly of MacrolobiumSchreb., an ecologically diverse Neotropical tree genus(Fabaceae-Detarioideae). Int. J. Plant Sci. 179: 75–86.

Nazareno, A. G., C.W. Dick & L. G. Lohmann. 2017.Wide butnot impermeable: Testing the riverine barrier hypothesis foran Amazonian plant species. Molec. Ecol. 26: 3636–3648.

Nesom, G. L., N. S. Fraga, W. R. Barker, P. M. Beardsley, D. C.Tank, B. G. Baldwin & R. G. Olmstead. 2019. Response to“The case for the continued use of the genus nameMimulusfor all monkeyflowers.” Taxon 68: 624–627.

Nevado, B., E. L. Y. Wong, O. G. Osborne & D. A. Filatov.2019. Adaptive evolution is common in rapid evolutionaryradiations. Curr. Biol. 29: 3081–3086.e5.

Nieder, J., S. Engwald, M. Klawun & W. Barthlott. 2000.Spatial distribution of vascular epiphytes (including hemi-epiphytes) in a lowland Amazonian rain forest (SurumoniCrane Plot) of southern Venezuela. Biotropica 32: 385–396.

Nogueira, A., P. J. Rey & L. G. Lohmann. 2012. Evolution ofextrafloral nectaries: Adaptive process and selective regimechanges from forest to savanna. J. Evol. Biol. 25: 2325–2340.

Nogueira, A., P. J. Rey, J. M. Alcantara, R. M. Feitosa & L. G.Lohmann. 2015. Geographic mosaic of plant evolution:Extrafloral nectary variation mediated by ant and herbivoreassemblages. PLoS ONE 10: e0123806.

Norris, W. R., D. Q. Lewis, M. P. Widrlechner, J. D. Thompson& R. O. Pope. 2001. Lessons from an inventory of the Ames,Iowa, flora (1859–2000). J. Iowa Acad. Sci. 108: 34–63.

Obermuller, F. A., M. Silveira, C. I. Salimon & D. C. Daly.2012. Epiphytic (including hemiepiphytes) diversity in threetimber species in the southwestern Amazon, Brazil. Bio-divers. & Conservation 21: 565–575.

Ohsawa, M., P. H. J. Nainggolan & N. Tanaka. 1985. Altitu-dinal zonation of forest vegetation on Mount Kerinci, Suma-tra: With comparisons to zonation in the temperate region ofeast Asia. J. Trop. Ecol. 1: 193–216.

Oleas, N. H., K. J. Feeley, J. Fajardo, A. W. Meerow, J.Gebelein & J. Francisco-Ortega. 2019. Muddy boots begetwisdom: Implications for rare or endangered plant speciesdistribution models. Diversity 11: 10. https://doi.org/10.3390/d11010010.

One Thousand Plant Transcriptomes Initiative. 2019. Onethousand plant transcriptomes and the phylogenomics ofgreen plants. Nature 574: 679–685.

Pace, M., L. G. Lohmann &W. Angyalossy. 2011. Evolution ofdisparity between the regular and variant phloem in Bigno-nieae (Bignoniaceae). Amer. J. Bot. 98: 602–618.

Pace, M. R., S. Alcantara, L. G. Lohmann & V. Angyalossy.2015. Secondary phloem diversity and evolution in Bigno-nieae (Bignoniaceae). Ann. Bot. 116: 333–358.

Paknia, O., H. Rajaei Sh & A. Koch. 2015. Lack of well-maintained natural history collections and taxonomists inmegadiverse developing countries hampers global biodiver-sity exploration. Organisms Diversity Evol. 15: 619–629.

Park, D. S., I. Breckheimer, A. C. Williams, E. Law, A. M.Ellison & C. C. Davis. 2018. Herbarium specimens revealsubstantial and unexpected variation in phenological sen-sitivity across the eastern United States. Philos. Trans., Ser.B 374: 20170394.

Pease, J. B., D. C. Haak, M. W. Hahn & L. C. Moyle. 2016.Phylogenomics reveals three sources of adaptive variationduring a rapid radiation. PLoS Biol. 14: e1002379.

Pendry, C. A. & J. Proctor. 1996. The causes of altitudinalzonation of rain forests on Bukit Belalong, Brunei. J. Ecol.84: 407–418.

Pennington, R. T. & C. W. Dick. 2010. Diversification of theAmazonian flora and its relation to key geological andenvironmental events: A molecular perspective. Pp. 373–385 in C. Hoorn & F. P. Wesselingh (editors), Amazonia,Landscape and Species Evolution. Blackwell, Oxford, UnitedKingdom.

Phillips, O. & J. S. Miller. 2002. Global Patterns of PlantDiversity: Alwyn H. Gentry’s Forest Transect Data Set.Monogr. Syst. Bot. Missouri Bot. Gard. 89.

Pinto, P. & P. M. Ruiz. 1984. Flora de Colombia. UniversidadNacional de Colombia, Bogota.

Pinto, R. B., B. M. Torke & V. Freitas de Mansano. 2012.Updates to the taxonomy of Swartzia (Leguminosae) in extra-Amazonian Brazil, with descriptions of five new speciesand a regional key to the genus. Brittonia 64: 119–138.

Volume 105, Number 32020

Lagomarsino & FrostTaxonomy in the Study of NeotropicalBiodiversity

419

Pirie, M. D., L. W. Chatrou, J. B. Mols, R. H. J. Erkens & J.Oosterhof. 2006. “Andean-centred” genera in the short-branch clade of Annonaceae: Testing biogeographical hy-potheses using phylogeny reconstruction and moleculardating. J. Biogeogr. 33: 31–46.

Pittier, H. 1908. Ensayo sobre las Plantas Usuales de CostaRica. H. L. & J. B. McQueen, Inc., Washington, D.C.

Polakowsky, H. 1879. Die Pflanzenwelt von Costa-Rica.Dresden.

Por, F. D. 2007. A “taxonomic affidavit”: Why it is needed?Integr. Zool. 2: 57–59.

Prata, E. M. B., C. Sass, D. P. Rodrigues, F. M. C. B. Domingos,C. D. Specht, G. Damasco, C. C. Ribas, et al. 2018. Towardintegrative taxonomy in Neotropical botany: Disentanglingthe Pagamea guianensis species complex (Rubiaceae). Bot.J. Linn. Soc. 188: 213–231.

Pupim, F. N., A. O. Sawakuchi, R. P. Almeida, C. C. Ribas, A.K. Kern, G. A. Hartmann, C. M. Chiessi, et al. 2019.Chronology of terra firme formation in Amazonian lowlandsreveals a dynamic Quaternary landscape. Quatern. Sci. Rev.210: 154–163.

Quijano-Abril, M. A., R. Callejas-Posada & D. R. Miranda-Esquivel. 2006. Distributional patterns and endemism areasof the Neotropical species of Piper (Piperaceae). J. Biogeogr.33: 1266–1278.

Rabeler, R. K., H. T. Svoboda, B. Thiers, L. A. Prather, J. A.Macklin, L. P. Lagomarsino, L. C. Majure, et al. 2019.Herbarium practices and ethics, III. Syst. Bot. 44: 7–13.

Reginato, M. 2016. monographaR: An R package to facilitatethe production of plant taxonomic monographs. Brittonia 68:212–216.

Renner, S. S. 1993. A history of botanical exploration inAmazonian Ecuador, 1739–1988. Smithsonian Contr. Bot.82: 1–39.

Rheindt, F. E., D. M. Prawiradilaga, H. Ashari, Suparno, C. Y.Gwee, G. W. X. Lee, M. Y. Wu, et al. 2020. A lost world inWallacea: Description of a montane archipelagic avifauna.Science 367: 167–170.

Ribas, C. C., A. Aleixo, A. C. R. Nogueira, C. Y. Miyaki & J.Cracraft. 2012. A palaeobiogeographic model for bioticdiversification within Amazonia over the past three millionyears. Proc. Biol. Sci. 279: 681–689.

Ricklefs, R. E. & F. He. 2016. Region effects influence localtree species diversity. Proc. Natl. Acad. Sci. U.S.A. 113:674–679.

Salazar, D., J. Lokvam, I. Mesones, M. Vasquez Pilco, J. M.Ayarza Zuñiga, P. de Valpine & P. V. A. Fine. 2018. Originand maintenance of chemical diversity in a species-richtropical tree lineage. Nat. Ecol. Evol. 2: 983–990.

Sangster, G. & J. A. Luksenburg. 2015. Declining rates ofspecies described per taxonomist: Slowdown of progress or aside-effect of improved quality in taxonomy? Syst. Biol. 64:144–151.

Sarkinen, T. & S. Knapp. 2016. Two new non-spiny Solanum(Solanaceae) from the Gran Chaco Americano and a key forthe herbaceous glandular-pubescent solanums from the re-gion. PhytoKeys 74: 19–33.

Sarkinen, T., L. Bohs, R. G. Olmstead & S. Knapp. 2013a. Aphylogenetic framework for evolutionary study of the night-shades (Solanaceae): A dated 1000-tip tree. BMC Evol. Biol.13: 214.

Sarkinen, T., P. Gonzales & S. Knapp. 2013b. Distributionmodels and species discovery: The story of a new Solanumspecies from the Peruvian Andes. PhytoKeys 31: 1–20.

Sarkinen, T., G. E. Barboza & S. Knapp. 2015a. True blacknightshades: Phylogeny and delimitation of the Morelloidclade of Solanum. Taxon 64: 945–958.

Sarkinen, T., S. Knapp & M. Nee. 2015b. Two new non-spinySolanum species from the Bolivian Andes (Morelloid Clade).PhytoKeys 47: 97–109.

Sauquet, H. & S. W. Graham. 2016. Planning the future ofplant systematics: Report on a special colloquium at theRoyal Netherlands Academy of Arts and Sciences. Amer.J. Bot. 103: 2022–2027.

Schindel, D. E. & J. A. Cook. 2018. The next generation ofnatural history collections. PLoS Biol. 16: e2006125.

Schlick-Steiner, B. C., F. M. Steiner, B. Seifert, C. Stauffer, E.Christian & R. H. Crozier. 2010. Integrative taxonomy: Amultisource approach to exploring biodiversity. Annual Rev.Entomol. 55: 421–438.

Sedio, B. E. 2017. Recent breakthroughs in metabolomicspromise to reveal the cryptic chemical traits that mediateplant community composition, character evolution and lin-eage diversification. New Phytol. 214: 952–958.

Sedio, B. E., J. R. Paul, C. M. Taylor & C.W. Dick. 2013. Fine-scale niche structure of Neotropical forests reflects a legacyof the Great American Biotic Interchange. Nat. Commun. 4:2317.

Shorthouse, D. P. & R. Page. 2019. Quantifying institutionalreach through the human network in natural history collec-tions. Biodivers. Inform. Sci. Standards 3: e35243.

Sklenar, P. 2006. Searching for altitudinal zonation: Speciesdistribution and vegetation composition in the superparamoof Volcan Iliniza, Ecuador. Pl. Ecol. 184: 337–350.

Snowden, J. D. 1933. A study in altitudinal zonation in southKigezi and on Mounts Muhavura and Mgahinga, Uganda.J. Ecol. 21: 7–27.

Sousa-Baena, M. S., N. R. Sinha & L. G. Lohmann. 2014.Evolution and development of tendrils in Bignonieae (Bigno-niaceae, Lamiales). Ann. Missouri Bot. Gard. 99: 323–347.

South, A. 2011. rworldmap: A new R package for mappingglobal data. R J. 3: 35–43.

Spooner, D. M., H. Ruess, C. I. Arbizu, F. Rodrıguez & C.Solıs-Lemus. 2018. Greatly reduced phylogenetic structurein the cultivated potato clade (Solanum section Petota proparte). Amer. J. Bot. 105: 60–70.

Standley, P. C. 1937. Flora of Costa Rica. Part I. Flora de CostaRica. Parte I. Field Mus. Nat. Hist., Bot. Ser. 18: 401–408.

Stern, S., L. Bohs, L. Giacomin, J. Stehman & S. Knapp. 2013.A revision of Solanum section Gonatotrichum. Syst. Bot. 38:471–496.

Stevens, W. D., C. Ulloa Ulloa, A. Pool & O. M. Montiel. 2001.Flora de Nicaragua. Monogr. Syst. Bot. Missouri Bot. Gard.85.

Strasser, B. J. 2019. Collecting Experiments: Making Big DataBiology. University of Chicago Press, Chicago.

Tancoigne, E. & A. Dubois. 2013. Taxonomy: No decline, butinertia. Cladistics 29: 567–570.

Taylor, D. W. 1991. Paleobiogeographic relationships ofAndean angiosperms of Cretaceous to Pliocene age. Palae-ogeogr. Palaeoclimatol. Palaeoecol. 88: 69–84.

Thode, V. A., I. Sanmartın&L. G. Lohmann. 2019. Contrastingpatterns of diversification between Amazonian and Atlanticforest clades of Neotropical lianas (Amphilophium, Bigno-nieae) inferred from plastid genomic data. Molec. Phylogen.Evol. 133: 92–106.

Tonduz, A. 1895. Exploraciones Botanicas en Talamanca:Informe Preliminar. Tipografia Nacional, San Jose, CostaRica.

Troudet, J., P. Grandcolas, A. Blin, R. Vignes-Lebbe & F.Legendre. 2017. Taxonomic bias in biodiversity data andsocietal preferences. Sci. Rep. 7: 9132.

Turrill, W. B. 1957. The subjective element in plant taxonomy.Bull. Jard. Bot. Etat. Bruxelles 27: 1–8.

420 Annals of theMissouri Botanical Garden

Uhlig, S. K. & K. Uhlig. 1991. Studies on the altitudinalzonation of forests and alpine plants in the Central BaleMountains, Ethiopia. Mt. Res. Dev. 11: 153–156.

Umaña, M. N. & N. G. Swenson. 2019. Intraspecific variationin traits and tree growth along an elevational gradient in asubtropical forest. Oecologia 191: 153–164.

van der Werff, H. & S. Nishida. 2010. Yasunia (Lauraceae), anew genus with two species from Ecuador and Peru. Novon20: 493–502.

Vellend, M., C. D. Brown, H. M. Kharouba, J. L. McCune &I. H. Myers-Smith. 2013. Historical ecology: Using uncon-ventional data sources to test for effects of global environ-mental change. Amer. J. Bot. 100: 1294–1305.

Villamil-Montero, D. A. & L. C. Ming. 2016. Las exploracionesbotanicas en Colombia: Una revision al legado botanicoliterario con analisis de las colecciones de Lamiaceae comoestudio de caso. Bol. Latinoamer. Caribe Pl. Med. Aromat.15: 128–135.

Vleminckx, J., D. Salazar, C. Fortunel, I. Mesones, N. Davila, J.Lokvam, K. Beckley, et al. 2018. Divergent secondarymetabolites and habitat filtering both contribute to treespecies coexistence in the Peruvian Amazon. Frontiers Pl.Sci. 9: 836.

von Humboldt, A. & A. Bonpland. 1807. Ideen zu einerGeographie der Pflanzen nebst einem Naturgemalde derTropenlander. Cotta, Tubingen.

Wagele, H., A. Klussmann-Kolb, M. Kuhlmann, G. Haszprunar,D. Lindberg, A. Koch & J. W. Wagele. 2011. The taxono-mist—An endangered race. A practical proposal for its sur-vival. Frontiers Zool. 8: 25.

Wang, X., R. L. Edwards, A. S. Auler, H. Cheng, X. Kong, Y.Wang, F. W. Cruz, et al. 2017. Hydroclimate changes acrossthe Amazon lowlands over the past 45,000 years. Nature541: 204–209.

Weeks, B. C., S. Claramunt & J. Cracraft. 2016. Integratingsystematics and biogeography to disentangle the roles ofhistory and ecology in biotic assembly. J. Biogeogr. 43:1546–1559.

Weese, T. L. & L. Bohs. 2007. A three-gene phylogeny of thegenus Solanum (Solanaceae). Syst. Bot. 32: 445–463.

Werner, Y. L. 2006. The case of impact factor versus taxonomy:A proposal. J. Nat. Hist. 40: 1285–1286.

Whaanga, H., W. Papa, P. Wehi & T. Roa. 2013. The use ofthe M�aori language in species nomenclature. J. Mar. IslandCultures. 2: 78–84.

Wheeler, Q. 2020. A taxonomic renaissance in three acts.Megataxa 1: 4–8.

Wiggins, I. L., D. M. Porter & E. F. Anderson. 1971. Flora ofthe Galapagos Islands. Stanford University Press, Stanford.

Wolf, J. H. D. & F.-S. Alejandro. 2003. Patterns in speciesrichness and distribution of vascular epiphytes in Chiapas,Mexico. J. Biogeogr. 30: 1689–1707.

Woodson, R. E. & R. W. Schery. 1980. Flora of Panama. Ann.Missouri Bot. Gard. 67: ii–xxxiii.

Xi, Z., B. R. Ruhfel, H. Schaefer, A. M. Amorim, M. Sugumaran,K. J. Wurdack, P. K. Endress, et al. 2012. Phylogenomicsand a posteriori data partitioning resolve the Cretaceousangiosperm radiation Malpighiales. Proc. Natl. Acad. Sci.U.S.A. 109: 17519–17524.

Yang, Z. 2015. The BPP program for species tree estimationand species delimitation. Curr. Zool. 61: 854–865.

Zapata, F. 2018. Dynamic monographs: Gateways to herbarium datafor the future.,https://hub.ki/groups/modernizingmonography..

Zapata, F. & I. Jimenez. 2012. Species delimitation: Inferring gapsin morphology across geography. Syst. Biol. 61: 179–194.

Zapata, F. & P. V. A. Fine. 2013. Diversification of themonoterpenesynthase gene family (TPSb) in Protium, a highly diverse genusof tropical trees. Molec. Phylogen. Evol. 68: 432–442.

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